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The Erythrina Gall Wasp Quadrastichus Erythrinae (Insecta: Hymenoptera: Eulophidae): Invasion History, Ecology, Infestation and Management

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The Erythrina Gall Wasp Quadrastichus Erythrinae (Insecta: Hymenoptera: Eulophidae): Invasion History, Ecology, Infestation and Management Review The Erythrina Gall Wasp Quadrastichus erythrinae (Insecta: Hymenoptera: Eulophidae): Invasion History, Ecology, Infestation and Management Sheng-Feng Lin 1 , Gene-Sheng Tung 2,* and Man-Miao Yang 1,* 1 Department of Entomology, National Chung Hsing University, Taichung 40227, Taiwan; sfl[email protected] 2 Division of Botanical Garden, Taiwan Forestry Research Institute, Taipei 100051, Taiwan * Correspondence: [email protected] (G.-S.T.); [email protected] (M.-M.Y.) Abstract: The Erythrina gall wasp Quadrastichus erythrinae Kim (Hymenoptera: Eulophidae) is an invasive insect that induces galls on coral trees (species of Erythrina, Fabaceae) in urban and suburban landscapes. Weakening and death of the tree were both observed after the infestation by this insect, wherein feeding and consequent draining of nutrients by a large population of Q. erythrinae could be playing a key role. In this article, we consolidate and summarize the information on the distribution, invasion route, ecology, infestation level, and management of Q. erythrinae populations in the last two decades and analyze the challenges in their management. Keywords: invasive insect; gall-inducing wasp; coral tree; urban tree Citation: Lin, S.-F.; Tung, G.-S.; Yang, 1. Introduction M.-M. The Erythrina Gall Wasp Quadrastichus erythrinae Kim is a gall-inducing wasp (Hymenoptera: Eulophidae) Quadrastichus erythrinae (Insecta: which was not known until year 2000, when it became a serious invasive pest [1]. This Hymenoptera: Eulophidae): Invasion tiny wasp (1–3 mm in body length) exhibits sexual dimorphism in body size and color History, Ecology, Infestation and (Figure1A) : males being smaller, white and brown; the females larger, orange and brown [1]. Management. Forests 2021, 12, 948. Quadrastichus erythrinae induces galls (Figure1B) on new flushes of leaves, young stems https://doi.org/10.3390/f12070948 and petioles of species of Erythrina that the infested trees wither and die. Many species of Erythrina were reported being attacked; for example, five species and a subspecies of coral Academic Editors: Rostislav Zemek trees are found affected in Taiwan, which are E. variegata L., E. variegata var. orientalis (L.) and Katarína Pastirˇcáková Merr., E. corallodendron L., E. cristagalli L., E. abyssinica Lam., and E. berteroana [2]. Erythrina includes about 130 species [3], which are generally confined to warmer parts of the world. Received: 11 June 2021 Many of them are planted as avenue trees due to its bright red and showy flowers and Accepted: 14 July 2021 Published: 18 July 2021 bright green thick foliage. Erythrina means ‘red’ in Greek, implying the color of their flowers. The bright-red flowers (Figure1C) bloom before new flushes of leaves appear, Publisher’s Note: MDPI stays neutral rendering the tree canopy appear red and hence popular as the ‘flame tree’ (Figure1D). with regard to jurisdictional claims in Erythrina sandwicensis exceptionally bears orange, yellow, salmon, green and white flow- published maps and institutional affil- ers [4,5]. Species of Erythrina are widely utilized by humans as ornamentals and some of iations. them have high ethnobotanical relevance [6–8]. Therefore, Q. erythrinae’s effect on various species of Erythrina gain in significance because Q. erythrinae populations alter the general appearance of Erythrina species with highly deformed foliage. The geographical spread of Q. erythrinae was discovered starting in the southern tropical hemisphere near Africa, later towards the subtropical and tropical areas of both southern and northern hemispheres Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. in Asia and Oceania, and further extended to the New World, which reveals an obvious This article is an open access article pattern of invasive dispersion in terms of time and geography. Two decades have passed distributed under the terms and since the discovery of Q. erythrinae, and it is time that we looked at what we have known conditions of the Creative Commons and learnt from the outbreak of this gall-inducing, invasive insect. In this article, we Attribution (CC BY) license (https:// review the invasion history, biology, ecology and current management of Q. erythrinae to creativecommons.org/licenses/by/ know how this insect could be better managed in future. We also analyze and discuss the 4.0/). challenges in the management of Q. erythrinae and provide possible management options. Forests 2021, 12, 948. https://doi.org/10.3390/f12070948 https://www.mdpi.com/journal/forests Forests 2021, 12, 948 2 of 13 Figure 1. Quadrastichus erythrinae Kim induced galls and Erythrina variegata L. (A) adult male (left) and female (right) wasps, (B) malformations (=galls), (C) red showy flowers of Erythrina variegata,(D) a blooming E. variegata. 2. Invasion History 2.1. Distribution Quadrastichus erythrinae has been reported in many tropical and subtropical nations (Table1). The species was described based on specimens reared from the malformations (hereafter, galls) on E. fusca Lour. in Singapore [1]. Furthermore, the insects extracted from the leaf galls on E. variegata in Mauritius in 2003 and on another unidentified species of Erythrina in Réunion in 2000 and 2003 were also examined in the same article. Later, the insect was reported invading other Asian countries and Pacific islands in neighborhoods such as Taiwan, Vietnam, Thailand, the Philippines, China, India, Japan, and Hawaii. It has also spread to the New World, including USA and Latin-American countries, such as Brazil, Mexico, and Panama. We synthesize a list of earliest recorded occurrence of Q. erythrinae in different localities, which consolidates information on its spread from the Old World to New World (Table1). Forests 2021, 12, 948 3 of 13 Table 1. Records of Quadrastichus erythrinae. Locality (Year of the Earliest Discovery) Hosts References Réunion (2000) Erythrina sp. Kim et al., 2004 [1] Seychelles (2002) E. variegata L. Gerlach and Madl, 2007 [9] Mauritius (2003) E. variegata L. (=E. indica) Kim et al., 2004 [1] Singapore (2003) E. fusca Lour. (=E. glauca) Kim et al., 2004 [1] E. variegata L., E. variegata var. orientalis (L.) Merr., E. corallodendron L., E. cristagalli Taiwan (2003) Yang et al., 2004 [2] L., E. abyssinica Lam., and E. berteroana Urban Thailand (2004) E. variegata L. EPPO 2021 [10] Faizal et al., 2006 [11]; Jacob and Devasahayam, 2010 [12]; Das and India (2005) Erythrina spp. Takukdar, 2011 [13]; Narayana and Dhanya, 2014 [14] Huang et al., 2005 [15]; Wu et al., China (2005) E. variegata L. 2008 [16]; Yao and Yin, 2009 [17] Uechi et al., 2007 [18]; Kanai et al., Japan (2005) E. variegata L. 2008 [19] Malaysia (2005) E. variegata L. Chung, 2006 [20] E. variegata L., E. crista-galli, E. Hawaii, USA (2005) Heu et al., 2008 [21] sandwicensis Florida, USA (2006) E. herbacea L. Howard et al., 2008 [22] Guam, USA (2006) Erythrina sp. Rubinoff et al., 2010 [23] Samoa (2006) E. variegata var. orientalis Rubinoff et al., 2010 [23] Sri Lanka (2006) Erythrina spp. Prathapan, 2006 [24] Vietnam (2007) E. variegata L. EPPO 2021 [10] Philippines (2010) E. variegata L. Lit et al., 2010 [25] French Polynesia (2010) E. variegata L. IPPC website, 2021 [26] E. variegata var. fastigiata, E. variegata var. Etienne and Dumbardon-Martial, Martinique (2012) orientalis, E. variegata var. variegata 2013 [27] E. variegata var. fastigiata, E. variegata var. Etienne and Dumbardon-Martial, Guadalupe (2012) orientalis, E. variegata var. variegata 2013 [27] Puerto Rico (2012) E. variegata L. Jenkins et al., 2014 [28] Brazil (2013) E. variegata L. Culik et al., 2014 [29] Mexico (2017) E. variegata L. Palacios-Torres et al., 2017 [30] Panama (2018) E. variegata L. Medianero and Zachrisson, 2019 [31] During early phases of this insect’s occurrences, Li et al. [32] predicted the potential invasion area of Q. erythrinae by the Genetic Algorithm for Rule Set Prediction based on insect incidence records and environmental data. The potential invasion area was deter- mined as 30◦ N and 35◦ S, and along coastal areas. Vegetation forms and humidity were predicted as critical factors for the spread of Q. erythrinae. They also suggested that Africa could be the site of origin. In their study, the potential area covered most of Q. erythrinae’s incidence from the world, and the Indian subcontinent was not included, which is where the insect was actually occurring before the paper was published. Later, more records were reported from not only the predicted invasion sites, but outside areas as well. For example, Medianero and Zachrisson [31] reported the occurrence of Q. erythrinae in Central Forests 2021, 12, 948 4 of 13 America, which was not predicted in Li et al. [32]. Therefore, the potential distribution of Q. erythrinae needs to be updated according to new information on distribution. 2.2. Tracing the Geographical Origin Identifying the exact origin of Q. erythrinae is not an easy task simply by the time of its occurrence because the early outbreak of Q. erythrinae seemed to happen in a short period of time in several southeastern Africa, Asian and Pacific countries (Table1)[ 1,9,10]. In 2000~2003, specimens from Réunion, Mauritius, Singapore and Taiwan were sent to the late John LaSalle (CSIRO, Canberra, Australia) to determine this gall-inducing insect. In 2004, it was described as a new species based on materials from Réunion, Mauritius, and Singapore [1] and later as a new record in Taiwan [2]. This gall-inducing wasp is apparently an invasive in Taiwan because it was not found before [2,33]. The spread of Q. erythrinae seems rapid not only in Taiwan, but also other warm parts of the world. In a few years, many countries had been invaded by Q. erythrinae, such as the Seychelles, Thailand, India, China, Japan (Okinawa), Malaysia, Sri Lanka, Vietnam, and the Philippines [10–20,24,25]. Severe infestations of Erythrina species by Q. erythrinae were reported from the Pacific islands also, such as Hawaii, Guam, Samoa, and French Polynesia [21,23,26].
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